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Environmental cadmium (Cd) sources have increased in mangrove sediments in recent decades, inducing cellular damage to many plants. Avicennia schaueriana is abundant in mangrove sites and has been subject to Cd contamination. The possible effects of Cd toxicity and the structural and physiological disturbances to this plant were studied. Can this plant express early cellular tolerance mechanisms to such metal contamination? Seedlings of A. schaueriana were collected from sites of their natural occurrence, placed in plastic pots containing nutrient solution for 60 days, and subsequently exposed to increasing Cd concentrations for 5 days under experimental conditions. The anatomical, ultrastructural and physiological changes induced by Cd were analysed. Cd accumulated mainly in the root system and in pneumatophores, stems and leaves, induced differential accumulation of mineral nutrients, but did not induce necrosis or changes in leaf anatomy. However, there was a decrease in starch grains and an increase in deposited electron-dense material in the cortex and vascular bundles. Cd induced both increases in calcium (Ca) content in shoots and Ca oxalate crystal precipitation in leaf mesophyll and was detected in crystals and in the secretion of salt glands. Our observations and experimental results provide evidence of Cd tolerance in A. schaueriana. As a new feature, despite the clear cellular physiological disorders, this plant is able to eliminate Cd through leaf salt glands and immobilise it in Ca crystals, representing fast mechanisms for Cd exclusion and complexation in leaves in heavy metal coastal polluted marine ecosystems.

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Mangroves have been subject to more metal contamination, including cadmium (Cd). This study evaluated if a relatively short Cd exposure may induce metabolic, morphological and ultrastructural cell disturbance in Avicennia schaueriana. Cd induced evident constraints to seedlings since there was reduction in leaf gas exchanges and the plants did not survive for more than 10 days at a higher Cd exposure in controlled conditions. The highest Cd accumulation was observed in roots and gradually less in stem and leaves. Cadmium induced lignin deposition was observed in xylem cells of all vegetative organs. Intense sclerification in xylem cells, endoderm and change in the hypoderm organization were also detected. Cadmium clearly induced chloroplast deformities with ruptures of its membranes, thylakoids and core and provoked cytoplasm disorganization. These metal constraints under natural conditions for long term can lead to the accumulation of cellular and metabolic damages and jeopardize seedlings establishment and local biodiversity.

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AbstractThe initial phase of a plant life cycle is a short and critical period, when individuals are more vulnerable to environmental factors. The morphological and anatomical study of seedlings and saplings leaf type enables the understanding of species strategies of fundamental importance in their establishment and survival. The objective of this study was to analyze the structure of seedlings and saplings leaf types of three mangrove species, Avicennia schaueriana, Laguncularia racemosa, Rhizophora mangle, to understand their early life adaptive strategies to the environment. A total of 30 fully expanded cotyledons (A. schaueriana and L. racemosa), 30 leaves of seedlings, and 30 leaves of saplings of each species were collected from a mangrove area in Guaratuba Bay, Paraná State, Brazil. Following standard methods, samples were prepared for morphological (leaf dry mass, density, thickness) and anatomical analysis (epidermis and sub-epidermal layers, stomata types, density of salt secretion glands, palisade and spongy parenchyma thickness). To compare leaf types among species one-way ANOVA and Principal Component Analysis were used, while Cluster Analysis evaluated differences between the species. We observed significant structural differences among species leaf types. A. schaueriana showed the thickest cotyledons, while L. racemosa presented a dorsiventral structure. Higher values of the specific leaf area were observed for seedlings leaves of A. schaueriana, cotyledons of L. racemosa and saplings leaves of A. schaueriana and R. mangle. Leaf density was similar to cotyledons and seedlings leaves in A. schaueriana and L. racemosa, while R. mangle had seedlings leaves denser than saplings. A. schaueriana and R. mangle showed hypostomatic leaves, while L. racemosa amphistomatic; besides, A. chaueriana showed diacytic stomata, while L. racemosa anomocytic, and R. mangle ciclocytic. Seedling leaves were thicker in R. mangle (535 µm) and L.racemosa (520 µm) than in A. schaueriana (470.3 µm); while saplings leaves were thicker in L. racemosa (568.3 µm) than in A. schaueriana seedlings (512.4 µm) and R. mangle (514.6 µm). Besides, seedlings leaves palisade parenchyma showed increasing thickness in L. racemosa (119.2 µm) <A. schaueriana (155.5 µm) <R. mangle (175.4 µm); while in saplings leaves as follows R. mangle (128.4 µm) <A. schaueriana (183.4 µm) <L. racemosa (193.9 µm). Similarly, seedlings leaves spongy parenchyma thickness values were as follows A. schaueriana (182.6 µm) = R. mangle (192.8 µm) <L. racemosa (354.4 µm); while in saplings were A. schaueriana (182.6 µm) = R. mangle (187.3 µm) <L. racemosa (331.3 µm). The analyzed traits, in different combinations, represent morphological adjustments of leaf types to reduce water loss, eliminate salt excess, increase the absorption of light, allowing a higher efficiency on the maintenance of physiological processes in this initial growth stage. Rev. Biol. Trop. 64 (1): 305-317. Epub 2016 March 01.

ResumenLa fase inicial del ciclo de vida de una planta es un período corto y crítico, cuando los individuos son más vulnerables a factores ambientales. El estudio morfológico y anatómico del tipo de hojas de las plántulas y árboles pequeños, permite la comprensión de las estrategias de las especies, que es de importancia fundamental para su establecimiento y supervivencia. El objetivo de este estudio fue analizar la estructura de los tipos de hojas de las plántulas y árboles pequeños de tres especies de mangle: Avicennia schaueriana, Laguncularia racemosa y Rhizophora mangle, para entender sus estrategias de vida tempranas de adaptación al ambiente. Un total de 30 cotiledones completamente abiertos (A. schaueriana y L. racemosa), 30 hojas de plántulas, y 30 hojas de árboles pequeños de cada especie se recolectaron en una área de manglar en Bahía Guaratuba, Estado de Paraná, Brasil. Siguiendo los métodos estándares, se prepararon muestras para análisis morfológicos (biomasa de hoja seca, densidad y espesor) y anatómicos (epidermis y capas sub-epidérmicas, tipos de estomas, densidad de glándulas secretoras de sal y grosor del parénquima empalizado y del esponjoso). Para comparar los tipos de hojas entre las especies se utilizaron un modelo lineal y Análisis de Componentes Principales, mientras que un análisis de conglomerados evaluó las diferencias entre las especies. Observamos diferencias estructurales significativas entre tipos de hoja en las especies. A.schaueriana mostró cotiledones más gruesos, mientras que L. racemosa presenta una estructura dorsiventral. Se observaron valores más altos del área foliar específica para las hojas de las plántulas de A. schaueriana, cotiledones de L. racemosa y hojas de árboles pequeños de A. schaueriana y R. mangle. La densidad de la hoja fue similar a la de los cotiledones y hojas de plántulas de A. schaueriana y L. racemosa, mientras que R. mangle tenía las hojas de las plántulas más gruesas que los árboles pequeños. A. schaueriana y R. mangle mostraron hojas hipostomáticas; L. racemosa anfiestomáticas; por otro lado A. chaueriana mostró estomas diacíticos, L. racemosa anomocíticos y R. mangle ciclocíticos. Las hojas de las plántulas eran más gruesas en R. mangle (535 micras) y L. racemosa (520 micras) que en A. schaueriana (470.3 m); mientras que las hojas de las plántulas eran más gruesas en L. racemosa (568.3 m) que en A. schaueriana (512.4 micras) y R. mangle (514.6 m). Además el parénquima empalizado de las plántulas mostró un aumento de espesor en L. racemosa (119.2 m) <A. schaueriana (155.5 m) <R. mangle (175.4 m); mientras que en las hojas de los árboles pequeños fue de siguiente manera: R. mangle (128.4 m) <A. schaueriana (183.4 m) <L. racemosa (193.9 m). Del mismo modo, en las hojas de las plántulas los valores del espesor del parénquima esponjoso fueron: A. schaueriana (182.6 m) = R. mangle (192.8 m) <L. racemosa (354.4 m); mientras que en los árboles pequeños: A. schaueriana (182.6 m) = R. mangle (187.3 m) <L. racemosa (331.3 m). Los rasgos analizados, en diferentes combinaciones, representan ajustes morfológicos de tipos de hojas para reducir la pérdida de agua, eliminar el exceso de sal, aumentar la absorción de la luz, lo que permite una mayor eficiencia en el mantenimiento de los procesos fisiológicos en esta etapa de crecimiento inicial.

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RESUMO

The initial phase of a plant life cycle is a short and critical period, when individuals are more vulnerable to environmental factors. The morphological and anatomical study of seedlings and saplings leaf type enables the understanding of species strategies of fundamental importance in their establishment and survival. The objective of this study was to analyze the structure of seedlings and saplings leaf types of three mangrove species, Avicennia schaueriana, Laguncularia racemosa, Rhizophora mangle, to understand their early life adaptive strategies to the environment. A total of 30 fully expanded cotyledons (A. schaueriana and L. racemosa), 30 leaves of seedlings, and 30 leaves of saplings of each species were collected from a mangrove area in Guaratuba Bay, Paraná State, Brazil. Following standard methods, samples were prepared for morphological (leaf dry mass, density, thickness) and anatomical analysis (epidermis and sub-epidermal layers, stomata types, density of salt secretion glands, palisade and spongy parenchyma thickness). To compare leaf types among species one-way ANOVA and Principal Component Analysis were used, while Cluster Analysis evaluated differences between the species. We observed significant structural differences among species leaf types. A. schaueriana showed the thickest cotyledons, while L. racemosa presented a dorsiventral structure. Higher values of the specific leaf area were observed for seedlings leaves of A. schaueriana, cotyledons of L. racemosa and saplings leaves of A. schaueriana and R. mangle. Leaf density was similar to cotyledons and seedlings leaves in A. schaueriana and L. racemosa, while R. mangle had seedlings leaves denser than saplings. A. schaueriana and R. mangle showed hypostomatic leaves, while L. racemosa amphistomatic; besides, A. chaueriana showed diacytic stomata, while L. racemosa anomocytic, and R. mangle ciclocytic. Seedling leaves were thicker in R. mangle (535 µm) and L. racemosa (520 µm) than in A. schaueriana (470.3 µm); while saplings leaves were thicker in L. racemosa (568.3 µm) than in A. schaueriana seedlings (512.4 µm) and R. mangle (514.6 µm). Besides, seedlings leaves palisade parenchyma showed increasing thickness in L. racemosa (119.2 µm) < A. schaueriana (155.5 µm) < R. mangle (175.4 µm); while in saplings leaves as follows R. mangle (128.4 µm) < A. schaueriana (183.4 µm) < L. racemosa (193.9 µm). Similarly, seedlings leaves spongy parenchyma thickness values were as follows A. schaueriana (182.6 µm) = R. mangle (192.8 µm) < L. racemosa (354.4 µm); while in saplings were A. schaueriana (182.6 µm) = R. mangle (187.3 µm) < L. racemosa (331.3 µm). The analyzed traits, in different combinations, represent morphological adjustments of leaf types to reduce water loss, eliminate salt excess, increase the absorption of light, allowing a higher efficiency on the maintenance of physiological processes in this initial growth stage.

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Confocal Laser Scanning Microscopy (CLSM) was used to observe sclereids from stems of Avicennia germinans and from fruits of two species of pear (Pyrus calleryana "Bradford" and P. communis "Red Bartlett"). The images obtained from thick (25 to 100 microm) free-hand sections were, in certain respects, far superior to those obtained by other, more invasive and time-consuming microscopic techniques upon which previous reports of sclereid morphology were based. The cell wall surfaces, including the "internal" surfaces of the branched pit canals and cell lumens, were much accentuated with the techniques we describe, resulting in a "fluorescence shell" image, meaning the cell wall did not stain all the way through but instead only at the inner and outer wall surfaces, including the edges of ramiform pits. By controlling the time of staining with 1% aqueous Safranin O, or by changing the number of optical sections used in extended focus images, it was possible to get either a conventional view of the cell wall structure or a unique, three-dimensional view of the elaborate cell interconnections. Similar fluorescence shell images of sclereids were also obtained using a periodic-Schiff (PAS) staining system, but the stain was not as specific to sclereid cell walls as was the Safranin O stain. Particularly with the use of a narrow range band pass emission filter of 505-530 nm, the Safranin O staining may be more specific to lignin than reported in the literature.

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